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A histopathologic study of extraction wounds in dogs
Oral pathology American
Academy
of Oral
Pathology
Donald Kerr, Editor
A histopathologic study of extraction wounds in dogs Raymond F. Huebsch, B.S., D.D.S.,” ad Louis S. Hawen,, D.D.S., M.S.,“# Sa?t Frawisco, Calif. SCHOOL
OF DENTISTRY,
UNIVERSITY
OF CALIFORNIA
T
he normal healing process following tooth extraction has been studied extensively in animals.l-U The histopathologic study of the healing process in disturbed extraction wounds, however, has not been conclusive. In 1921 Meyer1 studied disturbed extraction wounds in dogs by excising the surrounding gingiva, putting a grain of barley into the extraction wound, and placing a tampon in the alveolus after infecting the wound with st.aphylococci and streptococci. He found that the 12-day wounds showed a slight advancement in healing as compared to the undisturbed ones but that 6 and 18 days after extraction and infection there was no difference between the experimental and control wounds. Claflin,2 in 1936, demonstrated in dogs that healing of disturbed extraction wounds was delayed as compared with healing of wounds that had been undisturbed. He reported that dry sockets can be produced experimentally in dogs and that delayed healing, similar to “dry socket” in man, occurred spontaneously in dogs after the extraction of teeth. Ailing and Kerr3 c1emonstrate.d in monkeys that healing in dental sockets is delayed when the periodontal membrane is traumatized in the extraction procedure. Huebsch4 found that an adequate blood supply to the socket is necessary for normal healing in rats. Much has been written with respect to delay in healing of the infected alveolus. Schroff and BartelslO reported that they found fusiform bacilli and spirochetes in painful sockets with delayed healing. As soon as the pain ceased, these organisms were no longer found in the affected sockets. Belding and Beldingll found fusospirochetal organisms in all infected sockets. GrandstaP *Associate **Professor
Professor and Chairman, and Chairman, Section
Division of Oral Surgery. of Oral Pathology.
187
Pig. 1. Three days after surgical blood clot. (Magnification, x16.)
procedure.
Control
socket is filled
with
an organizing
Volume 28 Number 2
Extrclctio?L
u~ounds in dogs
189
Pi.g. B. Seven days after surgical procedure. Disturbed socket rcvcals that it is virtl dly )ty of the vascular granulation tissue seen in the rontrols. (Magnification, x13.) Fig. 3. Seven days after surgical procedure. Disturbed socket reveals resorption of the lieat bone Iining the socket {A), with new bone being laid down internal to the SUT,face 1. (Magnification, x155.)
(AS.,0.M. & 02. .4ugust,
1969
to rarious degrees, similar to the scrc~lxl dcgr~~(+3of alveolar osteitis in human patients. After postoperativcl intervals of II to 84 days, the sockets were resected cn bloc under general ancsthcsia and local infiltration of 2 per cent Iidocaine hydrachloride with 1 :lOO,OOOrpinrphrine. The tissues were fixed immediately in 10 per cent formalin, decalcified in I)ecal, and embedded in paraffin. Step seria1 sections were made stlgittslly and stainetl uith hetnatoxplin and cosin.
RESULTS Twenty-two of the experimental and control block sections were discarded from the study because the resulting sections were not of sufficient quality, were incapable of being properly oriented, were sectioned in the wrong plane, or because of other technical difficulties. Twenty experimental (disturbed) and eighteen control sockets (undisturbed) nmaincd for exxlnation. A consolidation of the microscopic findings follows. Three-day postoperathc i?tte>~~l. The control sockets were filled with an organizing blood clot (Fig. 1). The experimental sockets, revealed blood clots clinging to the mall of the socket. Excrpt~ for the amount of the blood clot, disturbed sockets were similar to the controls. Xeccw-day postoyerativc in ter2:al. The control sockets were filled with young
Pig. 4. Twelve to fourteen days after surgical procedure. Control tissue in which new bone is being laid down (A). fib] ‘011s connective x16.) lift ?rated across the socket (B). (Magnification,
socket is filled with Epithelium has pro-
Volume
28
Number
2
Extraction
wounds in dogs
191
Gg. 5. Twelve to fourteen days after surgical procedure. Disturbed socket is lin ed 71+th ulati on tissue (A) and contains both acute and chronic inflammatory ele me nts. CM ag1x 31.) Pig. 6. Twelve to fourteen days after surgical procedure. In the disturbed socket new bone is being laid down on the surface of the old bone (A). (Magnification, x12. j
On the ot~l~cr lranti, the disturbed sock&s rc~alctl typical “dry sockets” (Fig. ‘1) llistol):ttliologi(~~~~I;v, boric rcaorption was taking 1~1;1c~OH tllc ~nrfacc of the al\-colai~ 1)0n~k-I’oll~~ir~g SIIIY;I~~P ncvrosis. Xt. the fame illt(‘IWi~l to tll;lt SLLl*fijc(’ (Fig. 3). tinic, 11(‘\\- hO?llJ was being laitl do\\-rl Tlr~~l~,c-to Ii-dny posiop~r~lit~t i?licr?vls. The controls SOI*these prriods were fillctl completc1~ with poung fibrous conncctivc tissue in which new bone was being laid down (I34 g. 4). Although some of the disturbed sockets were cssentially empty, some rontaincd partial blood clots, pus, and debris. The sockets were linctl with granulation tissue n-hich containctl both acute and chronic inflammatory (~lc1~let~ts(Fig. 5). Kew honr \viIs being laid tlown on the stlrfi\cc of the old bone (Fig. 6). Trn ~t?y-one-tlay poutopcrutitv i~tcr1~17. Clontrol sockets wcrc filled or almost tomplctt~l~ filled with new bone, anti tht sock& openirr~~ ore covcretl with stratified syua~nous cpithelium (Fig. i) The c~spel.imr~ntal. sockets wcrc filled, tissue, nonvital but with various a.mounts of bloocl, tlebris, pus, granulation bollC frapmcnts, acUtc ant1 chronic illflill~ll~iltO~~~ Cells, ctr. (Fig. ‘i) Some Old boric \\‘ils undergoing rcmodrling ( Fig. X) . ~~crllflJ-‘i~ht-clay ~~~foy~rnti~*r infcrlqaf. Control sock&s were well healed, that is, fillctl with new boric ant1 covc~cd with surfaw epithelium (Fig. 9). The espcrimcntul or disturbc~l sockets wcrc filled with chronic granulation t,issue or loose, cdcmatous fibrous conncctivc tissue (Fig. 10). Twct/fy-fil*r- lo 56-duy pstoperntil~c i~~tc-rlds. The control sockets were well healcd. The tlisturbed sock&s wcrc filled xvitli loose, edematous fibrous connectivc t.isstic with now hone fornring on the socket. wall (Fig. 11 ) . The experimental sock& also contained clotted blootl, minute non]-ital bone spicnles, and other debris and \vvI’c likely to 11c iI~~Olll~~;l~li~~tl bJ- focal collrctions of iiiflammatoq cpithclimn c~vc~rctl the sockets, although it was not ~11s (Fig. 12). Suvfacc intact, and in places the rl~ithclium \\-a~ l~~l~ai~l~lastic~. ~YW~lll~ll~
pl~;l?l~1liltiO~l
tissnca.
DISCUSSION
F’orniation of a blood clot was the initial stage of tissue repair and regeneration in both groups. The disturbed sockets were lined with a thin blood clot. In the control sockets the blood clot, which filled the socket, became young v
Volume Number
28 2
Ex f m&on
wounds in dogs
Fig.
1
Fig.
193
7
8
Fig. 7. Twenty-one days after surgical procedure. Control sockets are alml 38t comply etc1y fille d wit ;h I lew bone (A). Note disturbed socket (B). (Magnification, x11.) days after surgical procedure. Bone lining the distul *bed socks:t is Fig. 8. Twenty-one Old bone is undergoing resorption (A), and new bone is being laid und lergoi w remodeling. (Magnification, x65.) dOV in on oP posite face (B).
cm,
0.x & 0.1’. August, 1969
days after surgical proccdurc>. Control sockets are corn4 el:ely fil lled Fig. 3. Twenty-eight x15.) with new bol ne (Ai. (Magnification, tissue or loor ;e, e‘demat OUS Fig. 10. The disturbed sockets are filled with c~hronic granulation x27.) fibrous CImm &ive tissue. (Magnification,
Volume Number
28 2
Extraction
wounds in dogs
E
195
12
Pig. 12. Thirty-five to fifty-six days after surgical procedure. The disturbed sockets filled with loose, edematous fibrous connective tissue, with new bone being formed on socket wall (A). (Magnification, x27.) Fig. 18. Thirty-five to fifty-six days after surgical procedure. Disturbed sockrts contai minute nonvital bone tissue and other debris, along with a focal collection of inflammat cells. Surface epithelium is hyperplastic. (Magnification, x16.)
are the ned ;ory
CONCLUSIONS
The healing process in distnrbetl al11I nndistnrbed sockets, is essentially parallel, except that in the disturbed sovkcts thcrr is delayed healing. In undisturbetl sock&s, new bone is laid clown directly on the alveolar boric lining t,hc socket and the sockets completely- regcneratc in 21 to 28 days. In disturbed sockets (“tlry sockets”), healing is dclaycd considerably. Initially, there is necrosis of the surface of the alveolar bone lining the socket. This is followed by resorption of that portion of the alveolar bone that, is necrotic. Eventually, resorption ceases and new bone begins to be laitl down on the remaining alveolar bone. In later sta.ges of healing, the nndisturbed sockets arc. well filled with bone. The central part of the disturbed soekcts, on the other hand, is filled with edematous connective tissue, bone spicnlcs, etc., which ctiscouragc healing with healthy fibrous connective tissue and boric. SUMMARY
The healing of forty-one extraction sites in dogs was interfered with by the use of gauze packs. The healing of these wounds was compared histopathologically at various postoperative intervals with healing in the same number of normal or undisturbed extraction wounds. REFERENCES w.: Die H&lung ran Extraktiorls~~untl~,n untcv almormrn VerhSiltnisscn, Ztsehr. Hto”nmto1. 22: 521-549, 1924. and Undisturlwd Extra&ion TVounds. J. Am. Dent. Claflin. R. 8.: Healing of Disturl,ed A. 23: 945-959, 1936. Alling, C. C., and Kerr, D. A.: Trauma as a Factor Causing Delayed Repair of Dental Extraction Sites, J. Oral Aurg. 15: 3-11, 1957. Huelwh, R. F.: Clinical and Histological Study of Alveolar Ostcitis, J. Oral Hurg. 16: 473482, 1958. Huctt~sch, IL F., Coleman, R. I)., %‘randsen, A. M., and Recks, H. : The Healing Process Male Rats (Long-Evans Strain), ORAL SURG., Following Molar Extraction. 1. Normal ORAL MED. & ORAL PATH. 5: 864-876, 1952. Study of Repair in th(x Maxillary Hones Following Surgery, Schram, W. R.: A Histologic .T. Am. Dent. A. 16: 1987-1997, 1929. IIul~l~c~ll, A. O., and Austin, I>. T.: Extraction Wounds and Therapeutic Agents: An Experimental Study, J. Am. Dent. A. 28: 251-258, 1941. Harrison, J. A.: Healing of Routine and Srvcwly Traumdtizcd Exodontia Wounds, Rur
1. McYcr,
2. 3. 4. 5. 6.
7. 8.
LI
43:
IOi-115,
194X.
Investigation Into the Healing of Extraction Lt’ounds in 9. Simpson, H. E.: Experimental Mawaus Rhesus Monkeys, J. Oral Surg. 18: 391-399, 1960. 10. Svhroff, J., and Rartvls, H. A.: Painful Rockets After Extractions; a Preliminary Report Prevention and Treatment, J. D. Res. 9: 81-88, on the Investigation of Their Etiology, 1929. 11. Bclding, P. H., and l+ltling, I,. .J. : I’ostcbxtraction lnfcctions : Preliminary Report on the Oral F~OTR, J. Am. Dent. A. 21: 1222-1237, 1934. 12. Grandstaff’, C. H.: The Influence of the Oral Bactc~ria on the Healing of Exodontia Wounds, Hur 35: 90-93, 1935.
Academy
of Oral
Pathology
Donald Kerr, Editor
A histopathologic study of extraction wounds in dogs Raymond F. Huebsch, B.S., D.D.S.,” ad Louis S. Hawen,, D.D.S., M.S.,“# Sa?t Frawisco, Calif. SCHOOL
OF DENTISTRY,
UNIVERSITY
OF CALIFORNIA
T
he normal healing process following tooth extraction has been studied extensively in animals.l-U The histopathologic study of the healing process in disturbed extraction wounds, however, has not been conclusive. In 1921 Meyer1 studied disturbed extraction wounds in dogs by excising the surrounding gingiva, putting a grain of barley into the extraction wound, and placing a tampon in the alveolus after infecting the wound with st.aphylococci and streptococci. He found that the 12-day wounds showed a slight advancement in healing as compared to the undisturbed ones but that 6 and 18 days after extraction and infection there was no difference between the experimental and control wounds. Claflin,2 in 1936, demonstrated in dogs that healing of disturbed extraction wounds was delayed as compared with healing of wounds that had been undisturbed. He reported that dry sockets can be produced experimentally in dogs and that delayed healing, similar to “dry socket” in man, occurred spontaneously in dogs after the extraction of teeth. Ailing and Kerr3 c1emonstrate.d in monkeys that healing in dental sockets is delayed when the periodontal membrane is traumatized in the extraction procedure. Huebsch4 found that an adequate blood supply to the socket is necessary for normal healing in rats. Much has been written with respect to delay in healing of the infected alveolus. Schroff and BartelslO reported that they found fusiform bacilli and spirochetes in painful sockets with delayed healing. As soon as the pain ceased, these organisms were no longer found in the affected sockets. Belding and Beldingll found fusospirochetal organisms in all infected sockets. GrandstaP *Associate **Professor
Professor and Chairman, and Chairman, Section
Division of Oral Surgery. of Oral Pathology.
187
Pig. 1. Three days after surgical blood clot. (Magnification, x16.)
procedure.
Control
socket is filled
with
an organizing
Volume 28 Number 2
Extrclctio?L
u~ounds in dogs
189
Pi.g. B. Seven days after surgical procedure. Disturbed socket rcvcals that it is virtl dly )ty of the vascular granulation tissue seen in the rontrols. (Magnification, x13.) Fig. 3. Seven days after surgical procedure. Disturbed socket reveals resorption of the lieat bone Iining the socket {A), with new bone being laid down internal to the SUT,face 1. (Magnification, x155.)
(AS.,0.M. & 02. .4ugust,
1969
to rarious degrees, similar to the scrc~lxl dcgr~~(+3of alveolar osteitis in human patients. After postoperativcl intervals of II to 84 days, the sockets were resected cn bloc under general ancsthcsia and local infiltration of 2 per cent Iidocaine hydrachloride with 1 :lOO,OOOrpinrphrine. The tissues were fixed immediately in 10 per cent formalin, decalcified in I)ecal, and embedded in paraffin. Step seria1 sections were made stlgittslly and stainetl uith hetnatoxplin and cosin.
RESULTS Twenty-two of the experimental and control block sections were discarded from the study because the resulting sections were not of sufficient quality, were incapable of being properly oriented, were sectioned in the wrong plane, or because of other technical difficulties. Twenty experimental (disturbed) and eighteen control sockets (undisturbed) nmaincd for exxlnation. A consolidation of the microscopic findings follows. Three-day postoperathc i?tte>~~l. The control sockets were filled with an organizing blood clot (Fig. 1). The experimental sockets, revealed blood clots clinging to the mall of the socket. Excrpt~ for the amount of the blood clot, disturbed sockets were similar to the controls. Xeccw-day postoyerativc in ter2:al. The control sockets were filled with young
Pig. 4. Twelve to fourteen days after surgical procedure. Control tissue in which new bone is being laid down (A). fib] ‘011s connective x16.) lift ?rated across the socket (B). (Magnification,
socket is filled with Epithelium has pro-
Volume
28
Number
2
Extraction
wounds in dogs
191
Gg. 5. Twelve to fourteen days after surgical procedure. Disturbed socket is lin ed 71+th ulati on tissue (A) and contains both acute and chronic inflammatory ele me nts. CM ag1x 31.) Pig. 6. Twelve to fourteen days after surgical procedure. In the disturbed socket new bone is being laid down on the surface of the old bone (A). (Magnification, x12. j
On the ot~l~cr lranti, the disturbed sock&s rc~alctl typical “dry sockets” (Fig. ‘1) llistol):ttliologi(~~~~I;v, boric rcaorption was taking 1~1;1c~OH tllc ~nrfacc of the al\-colai~ 1)0n~k-I’oll~~ir~g SIIIY;I~~P ncvrosis. Xt. the fame illt(‘IWi~l to tll;lt SLLl*fijc(’ (Fig. 3). tinic, 11(‘\\- hO?llJ was being laitl do\\-rl Tlr~~l~,c-to Ii-dny posiop~r~lit~t i?licr?vls. The controls SOI*these prriods were fillctl completc1~ with poung fibrous conncctivc tissue in which new bone was being laid down (I34 g. 4). Although some of the disturbed sockets were cssentially empty, some rontaincd partial blood clots, pus, and debris. The sockets were linctl with granulation tissue n-hich containctl both acute and chronic inflammatory (~lc1~let~ts(Fig. 5). Kew honr \viIs being laid tlown on the stlrfi\cc of the old bone (Fig. 6). Trn ~t?y-one-tlay poutopcrutitv i~tcr1~17. Clontrol sockets wcrc filled or almost tomplctt~l~ filled with new bone, anti tht sock& openirr~~ ore covcretl with stratified syua~nous cpithelium (Fig. i) The c~spel.imr~ntal. sockets wcrc filled, tissue, nonvital but with various a.mounts of bloocl, tlebris, pus, granulation bollC frapmcnts, acUtc ant1 chronic illflill~ll~iltO~~~ Cells, ctr. (Fig. ‘i) Some Old boric \\‘ils undergoing rcmodrling ( Fig. X) . ~~crllflJ-‘i~ht-clay ~~~foy~rnti~*r infcrlqaf. Control sock&s were well healed, that is, fillctl with new boric ant1 covc~cd with surfaw epithelium (Fig. 9). The espcrimcntul or disturbc~l sockets wcrc filled with chronic granulation t,issue or loose, cdcmatous fibrous conncctivc tissue (Fig. 10). Twct/fy-fil*r- lo 56-duy pstoperntil~c i~~tc-rlds. The control sockets were well healcd. The tlisturbed sock&s wcrc filled xvitli loose, edematous fibrous connectivc t.isstic with now hone fornring on the socket. wall (Fig. 11 ) . The experimental sock& also contained clotted blootl, minute non]-ital bone spicnles, and other debris and \vvI’c likely to 11c iI~~Olll~~;l~li~~tl bJ- focal collrctions of iiiflammatoq cpithclimn c~vc~rctl the sockets, although it was not ~11s (Fig. 12). Suvfacc intact, and in places the rl~ithclium \\-a~ l~~l~ai~l~lastic~. ~YW~lll~ll~
pl~;l?l~1liltiO~l
tissnca.
DISCUSSION
F’orniation of a blood clot was the initial stage of tissue repair and regeneration in both groups. The disturbed sockets were lined with a thin blood clot. In the control sockets the blood clot, which filled the socket, became young v
Volume Number
28 2
Ex f m&on
wounds in dogs
Fig.
1
Fig.
193
7
8
Fig. 7. Twenty-one days after surgical procedure. Control sockets are alml 38t comply etc1y fille d wit ;h I lew bone (A). Note disturbed socket (B). (Magnification, x11.) days after surgical procedure. Bone lining the distul *bed socks:t is Fig. 8. Twenty-one Old bone is undergoing resorption (A), and new bone is being laid und lergoi w remodeling. (Magnification, x65.) dOV in on oP posite face (B).
cm,
0.x & 0.1’. August, 1969
days after surgical proccdurc>. Control sockets are corn4 el:ely fil lled Fig. 3. Twenty-eight x15.) with new bol ne (Ai. (Magnification, tissue or loor ;e, e‘demat OUS Fig. 10. The disturbed sockets are filled with c~hronic granulation x27.) fibrous CImm &ive tissue. (Magnification,
Volume Number
28 2
Extraction
wounds in dogs
E
195
12
Pig. 12. Thirty-five to fifty-six days after surgical procedure. The disturbed sockets filled with loose, edematous fibrous connective tissue, with new bone being formed on socket wall (A). (Magnification, x27.) Fig. 18. Thirty-five to fifty-six days after surgical procedure. Disturbed sockrts contai minute nonvital bone tissue and other debris, along with a focal collection of inflammat cells. Surface epithelium is hyperplastic. (Magnification, x16.)
are the ned ;ory
CONCLUSIONS
The healing process in distnrbetl al11I nndistnrbed sockets, is essentially parallel, except that in the disturbed sovkcts thcrr is delayed healing. In undisturbetl sock&s, new bone is laid clown directly on the alveolar boric lining t,hc socket and the sockets completely- regcneratc in 21 to 28 days. In disturbed sockets (“tlry sockets”), healing is dclaycd considerably. Initially, there is necrosis of the surface of the alveolar bone lining the socket. This is followed by resorption of that portion of the alveolar bone that, is necrotic. Eventually, resorption ceases and new bone begins to be laitl down on the remaining alveolar bone. In later sta.ges of healing, the nndisturbed sockets arc. well filled with bone. The central part of the disturbed soekcts, on the other hand, is filled with edematous connective tissue, bone spicnlcs, etc., which ctiscouragc healing with healthy fibrous connective tissue and boric. SUMMARY
The healing of forty-one extraction sites in dogs was interfered with by the use of gauze packs. The healing of these wounds was compared histopathologically at various postoperative intervals with healing in the same number of normal or undisturbed extraction wounds. REFERENCES w.: Die H&lung ran Extraktiorls~~untl~,n untcv almormrn VerhSiltnisscn, Ztsehr. Hto”nmto1. 22: 521-549, 1924. and Undisturlwd Extra&ion TVounds. J. Am. Dent. Claflin. R. 8.: Healing of Disturl,ed A. 23: 945-959, 1936. Alling, C. C., and Kerr, D. A.: Trauma as a Factor Causing Delayed Repair of Dental Extraction Sites, J. Oral Aurg. 15: 3-11, 1957. Huelwh, R. F.: Clinical and Histological Study of Alveolar Ostcitis, J. Oral Hurg. 16: 473482, 1958. Huctt~sch, IL F., Coleman, R. I)., %‘randsen, A. M., and Recks, H. : The Healing Process Male Rats (Long-Evans Strain), ORAL SURG., Following Molar Extraction. 1. Normal ORAL MED. & ORAL PATH. 5: 864-876, 1952. Study of Repair in th(x Maxillary Hones Following Surgery, Schram, W. R.: A Histologic .T. Am. Dent. A. 16: 1987-1997, 1929. IIul~l~c~ll, A. O., and Austin, I>. T.: Extraction Wounds and Therapeutic Agents: An Experimental Study, J. Am. Dent. A. 28: 251-258, 1941. Harrison, J. A.: Healing of Routine and Srvcwly Traumdtizcd Exodontia Wounds, Rur
1. McYcr,
2. 3. 4. 5. 6.
7. 8.
LI
43:
IOi-115,
194X.
Investigation Into the Healing of Extraction Lt’ounds in 9. Simpson, H. E.: Experimental Mawaus Rhesus Monkeys, J. Oral Surg. 18: 391-399, 1960. 10. Svhroff, J., and Rartvls, H. A.: Painful Rockets After Extractions; a Preliminary Report Prevention and Treatment, J. D. Res. 9: 81-88, on the Investigation of Their Etiology, 1929. 11. Bclding, P. H., and l+ltling, I,. .J. : I’ostcbxtraction lnfcctions : Preliminary Report on the Oral F~OTR, J. Am. Dent. A. 21: 1222-1237, 1934. 12. Grandstaff’, C. H.: The Influence of the Oral Bactc~ria on the Healing of Exodontia Wounds, Hur 35: 90-93, 1935.